A simplified morphological classification scheme for pyramidal cells in six layers of primary somatosensory cortex of juvenile rats

Highlights • A simplified classification scheme for PCs by identifying apical dendritic morphology.• This classification scheme yielded 19 PC types cross all 6 layers of juvenile rat SSC.• Three aims are:• to introduce a simplified classification scheme for the PCs in different layers of SSC.• to present a full spectrum of various PCs based on a large amount of neurons reconstructed from SSC.• to reveal the structural organizing principles of PCs in different layers in a quantitative way.

[1]  J. W. Lewis,et al.  Two rules for callosal connectivity in striate cortex of the rat , 1995, The Journal of comparative neurology.

[2]  R. Ramos,et al.  Physiology and morphology of inverted pyramidal neurons in the rodent neocortex , 2013, Neuroscience.

[3]  Christof Koch,et al.  Adult Mouse Cortical Cell Taxonomy by Single Cell Transcriptomics , 2016, Nature Neuroscience.

[4]  R. Kötter,et al.  Cell Type-Specific Circuits of Cortical Layer IV Spiny Neurons , 2003, The Journal of Neuroscience.

[5]  R Kötter,et al.  Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer va in the primary somatosensory cortex. , 2006, Cerebral cortex.

[6]  H. Markram,et al.  Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. , 2002, Cerebral cortex.

[7]  R. Foehring,et al.  Morphological and electrophysiological properties of atypically oriented layer 2 pyramidal cells of the juvenile rat neocortex , 2000, Neuroscience.

[8]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  H. Markram,et al.  Anatomy and physiology of the thick-tufted layer 5 pyramidal neuron , 2015, Front. Cell. Neurosci..

[10]  Bob Jacobs,et al.  Regional Dendritic Variation in Primate Cortical Pyramidal Cells , 2002 .

[11]  R. Kötter,et al.  Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits , 2007, Brain Structure and Function.

[12]  Gordon M Shepherd,et al.  Opinion: an integrated approach to classifying neuronal phenotypes. , 2005, Nature reviews. Neuroscience.

[13]  J. Lübke,et al.  Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex , 2000, The Journal of Neuroscience.

[14]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[15]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  A. Sillito,et al.  Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  O. Ohana,et al.  Inter- and intralaminar subcircuits of excitatory and inhibitory neurons in layer 6a of the rat barrel cortex. , 2008, Journal of neurophysiology.

[18]  Andreas T. Schaefer,et al.  Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. , 2003, Journal of neurophysiology.

[19]  J. Brumberg,et al.  Morphological heterogeneity of layer VI neurons in mouse barrel cortex , 2009, The Journal of comparative neurology.

[20]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[21]  Edward M. Callaway,et al.  Retrograde Tracing with Recombinant Rabies Virus Reveals Correlations Between Projection Targets and Dendritic Architecture in Layer 5 of Mouse Barrel Cortex , 2007, Frontiers in neural circuits.

[22]  S. Buffer,et al.  Barreloids in adult rat thalamus: Three‐dimensional architecture and relationship to somatosensory cortical barrels , 1995, The Journal of comparative neurology.

[23]  S. Wise,et al.  Maturation of pyramidal cell form in relation to developing afferent and efferent connections of rat somatic sensory cortex , 1979, Neuroscience.

[24]  B. Sakmann,et al.  Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons , 2001, The Journal of physiology.

[25]  D. LaBerge,et al.  The cognitive significance of resonating neurons in the cerebral cortex , 2013, Consciousness and Cognition.

[26]  C. Radici,et al.  Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex , 1998, Neuroscience.

[27]  J. Bolz,et al.  Morphology of identified projection neurons in layer 5 of rat visual cortex , 1988, Neuroscience Letters.

[28]  J. Mendizabal-Zubiaga,et al.  The underside of the cerebral cortex: layer V/VI spiny inverted neurons , 2007, Journal of anatomy.

[29]  Paul Manger,et al.  Pyramidal cells in V1 of African rodents are bigger, more branched and more spiny than those in primates , 2013, Front. Neuroanat..

[30]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[31]  B. Sakmann,et al.  Three-dimensional axon morphologies of individual layer 5 neurons indicate cell type-specific intracortical pathways for whisker motion and touch , 2011, Proceedings of the National Academy of Sciences.

[32]  H. Markram,et al.  Dendritic calcium transients evoked by single back‐propagating action potentials in rat neocortical pyramidal neurons. , 1995, The Journal of physiology.

[33]  D. Feldmeyer.  Excitatory neuronal connectivity in the barrel cortex , 2012, Front. Neuroanat..

[34]  B Sakmann,et al.  Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. , 1995, The Journal of physiology.

[35]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

[36]  G. Snyder,et al.  A comparison of the electrophysiological properties of morphologically identified cells in layers 5B and 6 of the rat neocortex , 1992, Neuroscience.

[37]  Edward M. Callaway,et al.  Specialized Circuits from Primary Visual Cortex to V2 and Area MT , 2007, Neuron.

[38]  D. O'Leary,et al.  Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  Walther Akemann,et al.  Transgenic mice expressing a fluorescent in vivo label in a distinct subpopulation of neocortical layer 5 pyramidal cells , 2004, The Journal of comparative neurology.

[40]  J. Lübke,et al.  Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. , 2003, Cerebral cortex.

[41]  Edward M. Callaway,et al.  Excitatory Local Connections of Superficial Neurons in Rat Auditory Cortex , 2008, The Journal of Neuroscience.

[42]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets , 1994, The Journal of comparative neurology.

[43]  J. DeFelipe,et al.  High‐Resolution Light and Electron Microscopic Immunocytochemistry of Colocalized GABA and Calbindin D‐28k in Somata and Double Bouquet Cell Axons of Monkey Somatosensory Cortex , 1992, The European journal of neuroscience.

[44]  M. Diamond,et al.  Demonstration of discrete place‐defined columns—segregates—in the cat SI , 1990, The Journal of comparative neurology.

[45]  G. Elston,et al.  Neuronal composition and morphology in layer IV of two vibrissal barrel subfields of rat cortex. , 1997, Cerebral cortex.

[46]  Manuel Marx,et al.  Morphology and Physiology of Excitatory Neurons in Layer 6b of the Somatosensory Rat Barrel Cortex , 2012, Cerebral cortex.

[47]  H. Markram,et al.  Morphological Development of Thick-Tufted Layer V Pyramidal Cells in the Rat Somatosensory Cortex , 2011, Front. Neuroanat..

[48]  Edward M Callaway,et al.  Development of layer‐specific axonal arborizations in mouse primary somatosensory cortex , 2006, The Journal of comparative neurology.

[49]  E. White,et al.  Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex , 1986, The Journal of comparative neurology.

[50]  N. Spruston.  Neuroscience: Strength in numbers , 2008, Nature.

[51]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[52]  B. Connors,et al.  Regenerative activity in apical dendrites of pyramidal cells in neocortex. , 1993, Cerebral cortex.

[53]  Morphology of corticotectal cells in the primary visual cortex of hooded rats , 1987, The Journal of comparative neurology.

[54]  B. Sakmann,et al.  ‐Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex , 2002, The Journal of physiology.

[55]  B. Schofield,et al.  Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat , 1988, The Journal of comparative neurology.

[56]  B. Sakmann,et al.  Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[57]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[58]  Ingo Bojak,et al.  A gradual depth-dependent change in connectivity features of supragranular pyramidal cells in rat barrel cortex , 2014, Brain Structure and Function.

[59]  D. Tank,et al.  In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons , 1999, Nature Neuroscience.

[60]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[61]  F. Clascá,et al.  Long-range projection neurons of the mouse ventral tegmental area: a single-cell axon tracing analysis , 2015, Front. Neuroanat..

[62]  F. Valverde,et al.  Intrinsic neocortical organization: Some comparative aspects , 1986, Neuroscience.

[63]  Concha Bielza,et al.  Laminar Differences in Dendritic Structure of Pyramidal Neurons in the Juvenile Rat Somatosensory Cortex , 2016, Cerebral cortex.

[64]  Kathleen S Rockland,et al.  Collateral branching of long‐distance cortical projections in monkey , 2013, The Journal of comparative neurology.

[65]  B. Sakmann,et al.  Semi-automated three-dimensional reconstructions of individual neurons reveal cell type-specific circuits in cortex , 2011 .

[66]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[67]  Jennifer I. Luebke,et al.  Pyramidal Neurons Are Not Generalizable Building Blocks of Cortical Networks , 2017, Front. Neuroanat..

[68]  Wenjun Gao,et al.  Target‐specific differences in somatodendritic morphology of layer V pyramidal neurons in rat motor cortex , 2004, The Journal of comparative neurology.

[69]  Karl F. Jensen,et al.  Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex , 1988, Brain Research.

[70]  Karl Zilles,et al.  Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. , 2004, Cerebral cortex.

[71]  G. Shepherd,et al.  An integrated approach to classifying neuronal phenotypes , 2005, Nature Reviews Neuroscience.

[72]  Alex M Thomson,et al.  Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. , 2006, Cerebral cortex.

[73]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

[74]  Robert Miller,et al.  Theory of the normal waking EEG: from single neurones to waveforms in the alpha, beta and gamma frequency ranges. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[75]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[76]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties , 1994, The Journal of comparative neurology.

[77]  M. Deschenes,et al.  Intracortical Axonal Projections of Lamina VI Cells of the Primary Somatosensory Cortex in the Rat: A Single-Cell Labeling Study , 1997, The Journal of Neuroscience.

[78]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

[79]  N. Spruston.  Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[80]  Alex M. Thomson,et al.  Neocortical Layer 6, A Review , 2010, Front. Neuroanat..

[81]  B. Sakmann.  From single cells and single columns to cortical networks: dendritic excitability, coincidence detection and synaptic transmission in brain slices and brains , 2017, Experimental physiology.

[82]  Shaoqun Zeng,et al.  Visible rodent brain-wide networks at single-neuron resolution , 2015, Front. Neuroanat..

[83]  M. Deschenes,et al.  Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat , 2000, The Journal of comparative neurology.

[84]  Shane R. Crandall,et al.  A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses , 2015, Neuron.

[85]  B. Sakmann,et al.  Action potential initiation and propagation in rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[86]  E. Callaway,et al.  Three Types of Cortical Layer 5 Neurons That Differ in Brain-wide Connectivity and Function , 2015, Neuron.

[87]  Karel Svoboda,et al.  A platform for brain-wide imaging and reconstruction of individual neurons , 2016, eLife.

[88]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus , 1992, The Journal of comparative neurology.

[89]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[90]  Mark T. Harnett,et al.  Distribution and Function of HCN Channels in the Apical Dendritic Tuft of Neocortical Pyramidal Neurons , 2015, The Journal of Neuroscience.

[91]  H. S. Meyer,et al.  Cell Type–Specific Thalamic Innervation in a Column of Rat Vibrissal Cortex , 2010, Cerebral cortex.

[92]  H. Markram.  The Blue Brain Project , 2006, Nature Reviews Neuroscience.

[93]  Shaoqun Zeng,et al.  High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level , 2016, Nature Communications.

[94]  B. Connors,et al.  Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. , 2002, Journal of neurophysiology.

[95]  D. O'Leary,et al.  Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex , 1993, Neuron.

[96]  E. G. Jones,et al.  The organization and postnatal development of the commissural projection of the rat somatic sensory cortex , 1976, The Journal of comparative neurology.

[97]  Shawn R. Olsen,et al.  Gain control by layer six in cortical circuits of vision , 2012, Nature.

[98]  Farran Briggs,et al.  Organizing Principles of Cortical Layer 6 , 2009, Front. Neural Circuits.

[99]  H. Markram,et al.  Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. , 2007, Cerebral cortex.

[100]  Guy N Elston,et al.  Ipsilateral corticocortical projections to the primary and middle temporal visual areas of the primate cerebral cortex: area‐specific variations in the morphology of connectionally identified pyramidal cells , 2006, The European journal of neuroscience.

[101]  Shaul Hestrin,et al.  Layer 6 Corticothalamic Neurons Activate a Cortical Output Layer, Layer 5a , 2014, The Journal of Neuroscience.

[102]  Jens Hjerling-Leffler,et al.  Disentangling neural cell diversity using single-cell transcriptomics , 2016, Nature Neuroscience.

[103]  H. S. Meyer,et al.  Cell Type–Specific Three-Dimensional Structure of Thalamocortical Circuits in a Column of Rat Vibrissal Cortex , 2011, Cerebral cortex.

[104]  K. Rockland,et al.  Laminar distribution of neurons projecting from area V1 to V2 in macaque and squirrel monkeys. , 1992, Cerebral cortex.

[105]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[106]  J. DeFelipe,et al.  The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs , 1992, Progress in Neurobiology.

[107]  D. Simons,et al.  Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex , 1989, The Journal of comparative neurology.

[108]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  D. Feldmeyer,et al.  Morphological and physiological characterization of pyramidal neuron subtypes in rat medial prefrontal cortex. , 2015, Cerebral cortex.

[110]  S. Hestrin,et al.  Intracortical circuits of pyramidal neurons reflect their long-range axonal targets , 2009, Nature.

[111]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[112]  Ichiro Fujita,et al.  Pyramidal cell development: postnatal spinogenesis, dendritic growth, axon growth, and electrophysiology , 2014, Front. Neuroanat..

[113]  J. Winer,et al.  Columnar organization and reciprocity of commissural connections in cat primary auditory cortex (AI) , 1986, Hearing Research.

[114]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[115]  Shawn R. Olsen,et al.  Translaminar Inhibitory Cells Recruited by Layer 6 Corticothalamic Neurons Suppress Visual Cortex , 2014, Neuron.

[116]  S. Nelson,et al.  Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. , 2007, Journal of neurophysiology.

[117]  E. Jones.  Distribution patterns of individual medial lemniscal axons in the ventrobasal complex of the monkey thalamus , 1983, The Journal of comparative neurology.

[118]  Y. Kawaguchi.  Pyramidal Cell Subtypes and Their Synaptic Connections in Layer 5 of Rat Frontal Cortex , 2017, Cerebral cortex.